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Baffinellaceae Fam. Nov., Cryptophyceae) from Baffin Bay: Morphology, Pigment Profile, Phylogeny, and Growth Rate Response to Three Abiotic Factors1

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Baffinellaceae Fam. Nov., Cryptophyceae) from Baffin Bay: Morphology, Pigment Profile, Phylogeny, and Growth Rate Response to Three Abiotic Factors1 J. Phycol. *, ***–*** (2018) © 2018 Phycological Society of America DOI: 10.1111/jpy.12766 BAFFINELLA FRIGIDUS GEN. ET SP. NOV. (BAFFINELLACEAE FAM. NOV., CRYPTOPHYCEAE) FROM BAFFIN BAY: MORPHOLOGY, PIGMENT PROFILE, PHYLOGENY, AND GROWTH RATE RESPONSE TO THREE ABIOTIC FACTORS1 Niels Daugbjerg,2 Andreas Norlin Marine Biological Section, Department of Biology, University of Copenhagen, Universitetsparken 4, Copenhagen Ø DK-2100, Denmark and Connie Lovejoy Departement de Biologie, Universite Laval, 1045 avenue de la Medecine, Quebec, Quebec, G1V 0A6, Canada Twenty years ago an Arctic cryptophyte was Abbreviations: BA, Bayesian analysis; BS, bootstrap isolated from Baffin Bay and given strain number support; Cr-PC, cryptophyte-phycocyanin; Cr-PE, CCMP2045. Here, it was described using cryptophyte-phycoerythrin; ML, maximum likeli- morphology, water- and non-water soluble pigments hood; PP, posterior probability and nuclear-encoded SSU rDNA. The influence of temperature, salinity, and light intensity on growth rates was also examined. Microscopy revealed = typical cryptophyte features but the chloroplast Cryptophytes ( cryptomonads) are ubiquitous in color was either green or red depending on the marine and freshwater ecosystems worldwide and a few species have been recorded to form blooms light intensity provided. Phycoerythrin (Cr-PE 566) was only produced when cells were grown under (e.g., Laza-Martınez 2012, Supraha et al. 2014, and À À low-light conditions (5 lmol photons Á m 2 Á s 1). references therein). However, they also reside in Non-water-soluble pigments included chlorophyll a, more extreme environments, for example, soil (Paulsen et al. 1992), snow (Javornicky and Hindak c2 and five major carotenoids. Cells measured 8.2 3 5.1 lm and a tail-like appendage gave them a 1970), and inside ikaite columns (Ikka fjord, South- comma-shape. The nucleus was located posteriorly west Greenland; Kristiansen and Kristiansen 1999, and a horseshoe-shaped chloroplast contained a N. Daugbjerg, unpub. data). The currently accepted single pyrenoid. Ejectosomes of two sizes and a taxonomy of Cryptomonada includes two classes: nucleomorph anterior to the pyrenoid were the photoautotrophic Cryptophyceae (note: Chilomo- discerned in TEM. SEM revealed a slightly elevated nas is heterotrophic but this state is most likely sec- vestibular plate in the vestibulum. The inner ondarily derived) and the phagotrophic periplast component consisted of slightly Goniomonadea. Until recently, the latter class con- overlapping hexagonal plates arranged in 16–20 sisted of only a single genus Goniomonas and some oblique rows. Antapical plates were smaller and environmental sequences, but Shiratori and Ishida their shape less profound. Temperature and salinity (2016) have described the second heterotrophic studies revealed CCMP2045 as stenothermal and cryptomonad (Hemiarma marina). euryhaline and growth was saturated between 5 and The species diversity of Cryptophyceae has been À À 20 lmol photons Á m 2 Á s 1. The phylogeny based studied for more than 180 years as Ehrenberg dis- on SSU rDNA showed that CCMP2045 formed a covered the first cryptophyte (Cryptomonas ovata)in distinct clade with CCMP2293 and Falcomonas sp. 1831. However, the first detailed descriptions and isolated from Spain. Combining pheno- and drawings were published 7 years later (Ehrenberg genotypic data, the Arctic cryptophyte could not be 1838). According to AlgaeBase, as of May 2018, placed in an existing family and genus and there are 41 genera listed in the Cryptophyceae (Guiry and Guiry 2018) and of these 21 are mono- therefore Baffinellaceae fam. nov. and Baffinella = frigidus gen. et sp. nov. were proposed. typic ( 53.7%). At the biochemical level, cryptophytes possess a Key index words: Arctic flagellates; cryptophytes; unique combination of pigments that include growth rates; phylogeny; taxonomy; ultrastructure chlorophylls a and c2, one of two phycobiliproteins and the cryptophyte specific carotenoid alloxanthin, alongside other common carotenoids (Hill and Rowan 1989, Cerino and Zingone 2007, Egeland 1 Received 17 April 2018. Accepted 27 June 2018. First Published 2016). The two phycobiliproteins found in crypto- Online 25 July 2018. 2Author for correspondence: e-mail [email protected]. phytes are phycoerythrin and phycocyanin, and Editorial Responsibility: L. Graham (Associate Editor) these have different structural configurations 1 2 NIELS DAUGBJERG ET AL. identified by their absorption peaks. Some of these with existing families. Thus, a new family Baffinel- configurations are unique (Hill and Rowan 1989, laceae fam. nov. was also described. Novarino 2012). For each genus, only one type of phycobiliprotein is present except for Hemiselmis that has been shown to contain species with either MATERIALS AND METHODS Cr-PC 615 and Cr-PE 555 (Hill and Rowan 1989). Culture. Strain CCMP2045 was isolated from a water sam- 0 As some families possess the same phycobiliprotein ple collected in Baffin Bay (June 23, 1998; 76°19 15″ N, ° 0 ″ (Clay et al. 1999), it has been discussed if the pho- 75 49 02 W; Fig. 1) at a depth of 11 m. A sub-culture of this tosynthetic pigment profile can be used to distin- strain was sent to the Marine Biological Section at University of Copenhagen where it has been kept at 4°C in L1 medium guish taxa at the family level (Fritsch 1935, (Guillard and Hargraves 1993) with a salinity of 30 and a Pringsheim 1944, Butcher 1967, Hill and Rowan light:dark cycle of 16:8 h. 1989). Microscopy. Live cells were studied using a Carl Zeiss Axio At the light microscopical level, the gross mor- Imager.M2 with a 639 oil immersion lens. Micrographs were phology of cryptophytes is somewhat similar: droplet taken with a Zeiss AxioCam HRc digital camera (Zeiss, Ober- cell shape and two flagella that emerge from the kochen, Germany). Chlorophyll fluorescence was recorded subapical end. Thus, most taxonomic differences using a Zeiss AxioCam MRc digital camera and the filter set 09 (excitation BP450-490, emission LP515). Length and width relate to the ultrastructure of the periplast compo- of 59 cells were measured using Zen image acquisition soft- nent, position of the nucleomorph, appearance of ware from Zeiss. Means and standard deviations were calcu- the rhizostyle, and the furrow-gullet complex (Clay lated using IBM SPSS statistics (ver. 24, Armonk, NY, USA). et al. 1999). For transmission electron microscopy, 5 mL of a dense cul- In the Arctic, cryptomonads have been shown to ture was fixed in 5 mL of 4% glutaraldehyde in 0.2 M cacody- contribute to both pelagic and sympagic communi- late buffer containing 0.5 M sucrose for 1 h and 25 min. The ties of microalgae. They are also part of the spring fixed cells were pelleted by centrifugation and the super- natant except for 2 mL was removed. Two milliliter 0.2 M bloom when the sea ice melts and nutrients are cacodylate buffer containing 0.5 M sucrose was added. After released to the open water column (Mikkelsen 20 min, 2 mL of the supernatant was removed and replaced et al. 2008, Vallieres et al. 2008, Poulin et al. 2011, with 2 mL 0.2 M cacodylate buffer without sucrose for Coupel et al. 2012). However, very few studies have 20 min. The mix was centrifuged at 1,201 g for 10 min after addressed the taxonomy of Arctic cryptophytes. each of these steps. For post-fixation 2 mL of the supernatant Recently, the species diversity of Arctic marine pro- tists including cryptomonads was studied by molec- ular techniques (e.g., clone libraries and high throughput sequencing; Sørensen et al. 2012, Mar- quardt et al. 2016, Stecher et al. 2016). These stud- ies have provided detailed information on operational taxonomic units, but for many of the determined ribotype sequences we have little understanding of the corresponding morphos- pecies. In this study, a cryptophyte was isolated from material collected in Baffin Bay in Arctic Canada (1998), and later deposited at Provasoli-Guillard National Center for Marine Micro Algae and Micro- biota in Maine, USA (Potvin and Lovejoy 2009), where it was given the strain number CCMP2045. The aim of this study was to describe this strain using a polyphasic approach, which included a mor- phological characterization using LM, TEM and SEM. The composition of both water and non-water- soluble pigments was analyzed to describe the pro- file of photosynthetic marker pigments. To infer the phylogeny of CCMP2045, the nuclear-encoded SSU rDNA sequence was compared to 50 other cryp- tomonads. Finally, growth rates were estimated through autecological experiments elucidating salin- ity and temperature tolerance limits as well as growth rates at different light intensities. Based on these results, a new genus and species Baffinella frigi- dus gen. et sp. nov. was proposed to accommodate for strain CCMP2045. The combination of morpho- FIG. 1. Map of sampling location (*)ofBaffinella frigidus gen. logical features and phycobiliproteins did not fit et sp. nov. in Baffin Bay. BAFFINELLA FRIGIDUS, AN ARTIC MARINE CRYPTOPHYTE 3 was removed and 2 mL, consisting of 0.5 mL 4% OsO4 and previously been determined by Potvin and Lovejoy. The 1.5 mL 0.2 M cacodylate buffer was added for 1 h before sequences were retrieved from GenBank (accession number being rinsed with 0.2 M cacodylate buffer. For dehydration, a GQ375264 and GQ375265, respectively) and added to an series of ethanol was used, 20 min for each concentration alignment consisting of 50 other SSU rDNA sequences of (30%, 50%, 70%, 90%, and 100% in molecular sieves) with cryptomonads including 18 genera and 38 taxa identified to 100% in molecular sieves used twice. The pellet was rinsed species. The data matrix was edited using the JALVIEW twice in propylene oxide before embedding and left over- sequence editor (ver. 2.9.0b2; Waterhouse et al. 2009) follow- night in a mix of 1:1 propylene oxide and Spurr’s resin. The ing an alignment based on ClustalW as implemented in the next day Spurr’s resin was replaced by fresh Spurr’s resin for software.
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